HORTSCIENCE 39(3):553–557. 2004. isolates from four cultivars to determine the susceptibility of each cultivar to the four iso- lates. Isolates differed in their ability to form Pathogenic Variation of subcuticular hyphae on the different cultivars, with the greatest amount of infection usually caryigenum Isolates and Corresponding occurring when the isolate was placed back onto the cultivar from which it was isolated. Differential Resistance in It is apparent from these studies that a range of genetic or pathotypes of C. caryige- Patrick J. Conner1 num exist that differ markedly in their ability Department of Horticulture, University of Georgia, Coastal Plain Experiment to cause disease on different pecan cultivars. Station, 4604 Research Way, Tifton, GA 31793 The work reported here was undertaken to further examine the extent of pathogenic Katherine L. Stevenson variation among scab isolates using a larger Department of Plant Pathology, University of Georgia, Athens, GA 30602-7274 number of cultivars and fungal isolates. These results may be useful in designing crosses to Additional index words. Carya illinoinensis, scab, vertical resistance, , histology pyramid resistance genes into a single cultivar or in selecting combinations of cultivars to be Abstract. To facilitate the breeding of scab-resistant pecan [Carya illinoinensis (Wangenh.) included in an orchard. C. Koch] cultivars, more information is needed about the pathogenic variation of the causal organism, Cladosporium caryigenum (Ell. et Lang.) Gottwald (1982). This study examined Materials and Methods the virulence patterns resulting from the field inoculations of 19 pecan cultivars with 12 monoconidial isolates from 8 pecan cultivars at 7 locations. The virulence pattern was Inoculum preparation. Twelve isolates from different for each of the fungal isolates. Each isolate was virulent on some cultivars and eight pecan cultivars and seven locations were avirulent on others. Most isolates were most virulent on the cultivar of their origin and used in the study (Table 1). Frozen stocks of one or a few other cultivars. Several cultivars were resistant to most of the tested isolates. monoconidial scab isolates were prepared ac- The results indicate a large pool of differential and ephemeral resistance to scab resides cording to Conner (2002). Isolates used in the in the pecan germplasm. Microscopic examination of developing lesions suggests that experiment were revived from frozen stocks resistance is mediated by the speed of plant cell wall modifications that limit the growth by placing filter paper discs with the dried of subcuticular hyphae. This information will be useful in the selection of cultivars with germinated conidia directly onto oatmeal agar functionally different resistance genes for use in designing cultivar mixtures or in breed- plates. After 2 weeks of incubation at 24 °C in ing programs. the dark, the fungal colonies were homogenized in sterile water and spread across a fresh oat- The pecan scab fungus is the most economi- resistance. Unfortunately, this resistance has meal agar plate that was again incubated for 2 cally damaging pathogen of pecan in the humid collapsed and now both cultivars are considered weeks at 24 °C. Subsections of this plate were growing conditions of the southeastern U.S. susceptible. The appearance and spread of a homogenized in water and spread onto oatmeal Foliar infections result in black circular lesions race of the fungus capable of infecting ‘Stuart’ agar plates to produce conidia for inoculations. that under favorable conditions can result in has been documented in the literature (Cole After 1 to 2 weeks growth at 24 °C, conidia severe leaf spotting, premature defoliation, and Gossard, 1956). were harvested by flooding cultures with 2 ml and shoot death. Development of lesions on The impermanence of cultivar resistance to of sterile water and the concentration adjusted fruit shucks reduces yield and nut quality, and scab infections can be explained by variation to 1 × 106 conidia/mL. if not controlled it can result in total crop loss in populations of C. caryigenum. Differences Inoculation. The cultivars chosen for this (Sanderlin, 1994). Commercial pecan plantings in virulence among scab isolates were first study represent a wide range of currently may require up to 11 fungicide applications reported by Demaree and Cole (1929) who popular or historically important cultivars. annually to control the disease (Ellis et al., used orchard inoculations to demonstrate that Trees were grown in an orchard located at the 2000). Pecan scab has developed resistance at least four races of the pathogen existed that Coastal Plain Experiment Station in Tifton, Ga. to at least one common fungicide, benomyl differed in their ability to infect pecan cultivars. All trees received recommended fertilization (Sanderlin, 1992), and recent concerns over Further testing demonstrated the presence of and supplemental irrigation (Crocker, 1996). negative environmental health effects of at least four races based on their pathogenicity No fungicides were applied to the orchard pesticides has increased pressure to restrict on four pecan cultivars in the greenhouse and during the course of this experiment. valuable control agents (Guillebeau, 1998). The the field (Converse, 1960). Bracewell (1996) Inoculations were made by spraying ex- development of scab resistant cultivars with found cultivar-inoculum source interaction was panding shoots with a conidial suspension of excellent commercial quality would greatly significantly associated with disease intensity. C. caryigenum until runoff using a spray bottle. increase the profitability of pecan cultivation Using a detached leaf assay, Conner (2002) Each shoot consisted of five to ten compound in the southeastern U.S. and it is the focus of examined microscopically four C. caryigenum leaves and each leaf consisted of 5 to 13 leaflets several cultivar development programs (Con- ner, 1999; Goff et al., 1998; Thompson and Table 1. Sources of isolates of Cladosporium caryigenum used in study. Grauke, 1994). a Effective breeding for resistance to Clado- Isolate Year Host cultivar Location sporium caryigenum requires information on Cf-Au-2 1999 Cape Fear Lee, Ala. De-Tif-3 1999 Desirable Tift, Ga. the pathogenic diversity of the fungus. Many De-Mo-11 1999 Desirable Jefferson, Fla. cultivars that were once highly resistant to scab AL-LI-DE 2000 Desirable Lee, Ala. are now widely considered susceptible. For GA-FW-DE 2000 Desirable Dougherty, Ga. example, ‘Desirable’ and ‘Stuart’ are grown LA-MP-DE 2000 Desirable Natchitoches Par, La. throughout the Southeast and were initially Fa-Tif-11 2001 Farley Tift, Ga. popular in part due to their high levels of scab Ma-Tif-11 2001 Mahan Tift, Ga. Pa-OK-11 2000 Pawnee Payne, Okla. Sc-Tif-1 1999 Schley Tift, Ga. Received for publication 24 Feb. 2003. Accepted St-Tif-13 2001 Stuart Tift, Ga. for publication 23 June 2003. 1Corresponding author; e-mail pconner@tifton. Wi-Tif-2 1999 Wichita Tift, Ga. cpes.peachnet.edu. aCounty or parish, state.

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were treated in the same manner except that Results and discussion leaves were sprayed with sterile water. No lesions were produced in any of the control Field inoculation of pecan trees is chal- inoculations so this data was omitted from lenging because of the large plant size and the results. Leaves were collected 28 d after the requirement for free moisture during inoculation and all leaflets were examined for the initial infection period (Turechek and the presence of scab lesions. Disease severity Stevenson, 1998). Greenhouse inoculations was assessed on individual leaflets on a scale were not attempted due to the difficulty of of 1 to 4, where 1 = no visible symptoms, 2 obtaining plant material of suitable size and = pin-point necrotic lesions with sparse or no because greenhouse inoculations often do sporulation, 3 = chlorotic lesions with limited not sporulate as readily as field inoculations expansion and sporulation, and 4 = large dark (Converse, 1960). expanding lesions with abundant sporulation. Inoculations produced a range of symptoms Shoots were scored as the most severe rating on host leaves varying from small pinpoint le- observed on any leaflet. The entire experiment sions to the large spreading dark lesions typical Fig. 1. Typical symptoms induced by artificial inocu- was repeated for a total of two trials for each of natural scab infections (Fig. 1). Disease lation of Cladosporium caryigenum on different cultivar–isolate combination. reactions were categorized based on the most pecan hosts. (A) Isolate De-Tif-3 on the cultivar Microscopic examination. For microscopic severe reaction observed on any leaflet on the ‘Mahan’ showing a type 2 intermediate reaction examination of disease progress, four isolates treated shoot. This avoided the bias that could with pin-point lesions with sparse or no sporula- of C. caryigenum, Fa-Tif-11, De-Tif-3, Pa- be introduced by the beginning of ontogenic tion. (B) Isolate De-Tif-3 on ‘Cape Fear’ showing OK-11, and Wi-Tif-2, were used to inoculate resistance in the more mature basal leaflets or a type 3 intermediate reaction with chlorotic by inoculum falling off some leaves resulting lesions with limited expansion and sporulation. leaves of ‘Farley’ in the field using the methods (C) Isolate De-Tif-3 on ‘Desirable’ showing a described above. Whole leaf mounts were used in a shifting of the score to the lower end of type 4 susceptible reaction with large expanding to observe disease progression over a 2-week the scale. By consistently taking the worst case lesions and abundant sporulation. period. A 1-cm2 section was cut from the center observed, the results were biased towards the of the leaflet for each sample. Samples were hypothesis of all cultivars susceptible to all that varied in maturity from most mature at the stained with trypan blue and chlorazol Black isolates. However, reaction scores were rela- base to newly formed leaflets at the tip. Thus, E according to Conner (2002). Leaves were tively consistent between replicate inoculations for each inoculated shoot a minimum of 20 sampled at 2, 4, 7, 11, and 15 d postinocula- with the majority of ratings being equal and leaflets were still expanding and susceptible tion. Eight leaflets for each isolate / time period differences usually separated by only a single to infection at the time of inoculation. Leaves were examined. On each sample 25 germinated class (Table 2). were then wrapped loosely with a moist conidia were examined for the presence of sub- Leaves producing no visible symptoms paper towel and enclosed in aluminum foil cuticular hyphae, reproductive initials, and halo were considered to be resistant to the chal- to reflect sunlight. Leaves were covered for staining of the nearby epidermal cells. Thus, lenging isolate. Leaves producing a type 4 48 h and then uncovered to dry. The tested 200 germinated conidia were observed for reaction, with its typical expanding lesion, cultivars always included the original cultivar each data point. Differences in fungal growth abundant sporulation, and surrounding green host for each isolate. This served as a general among C. caryigenum isolates at each time host tissue were considered susceptible to the control to assure that the inoculum was viable period were determined statistically by one challenging isolate. Reaction types falling and virulent. Noninoculated control shoots way analysis of variance (SigmaStat). between these two extremes were categorized Table 2. Symptomsz caused by differential isolates of Cladosporium caryigenum on pecan cultivars. Host of origin and identity of inoculated isolates Cape Fear Desirable Farley Mahan Pawnee Schley Stuart Wichita Test cultivar Cf-Au-2 De-Tif-3 De-Mo-11 AL-LI-DE GA-FW-DE LA-MP-DE Fa-Tif-11 Ma-Tif-11 Pa-OK-11 Sc-Tif-1 St-Tif-13 Wi-Tif-2 Barton 1y 1 1 1 1 1 1,2 1 1 1 1 1 Cape Fear 4 3 2,3 3 2,3 1 1 1 2,3 1 1 2 Cheyenne 1 3 2,3 3 1,2 1 1 1 1 1 1 1 Curtis 1 1,2 1 1 1 1 1 1 1 1 1 1 Desirable 1 4 4 4 4 1 1 1 1 1* 1 1 Elliot 1 2,3 2,3 NTx 1 NT 1 1 1 1 1 1 Farley 1 2 3 3 3 3 4 2* 2,3 1 3 1 Gloria Grande 1 1,2 2* 1 1 1 1,2 1 1 1 2 1 Kiowa 1 3 3 3 1 4 1,2 4 2,3 1 1 2 Mahan 2,3 2 2 2 1 4 1,3 4 2,3 1,2 1,2 2 Money Maker 1,2 3 3 1 NT NT 4 3 3* 2,3 2* 3 Pawnee 3 2 1,2 3 3 1 1 2 4 1 3,4 2 Schley 1 2 2,3 3 1 4 2,3 4 3 4 1 4 Shoshoni 1 3 1,3 3 3 2 1 1 1,2 1 3,4 1 Stuart 1 1 1 1 1 1 1 2 1 1 3* 1 Sumner 1 1 1 2 1 1 1 1 1 1 1 1 Wichita 1 2,3 1,2 2* NT 4 4 4 4 1,2 1* 4 Woodard 1 3 2* 3,4 3 3,4 3 3 2,3 1 1 1,2 No. susceptiblew 1 1 1 2 1 5 3 4 2 1 2 2 No. intermediatev 3 14 13 10 6 2 6 5 8 3 5 6 No. resistantu 14 3 4 5 9 9 9 9 8 14 11 10 zSymptoms: 1 = no visible symptoms; 2 = pinpoint lesions with no or sparse sporulation; 3 = chlorotic lesions with reduced expansion and sporulation; 4 = large spreading lesions with abundant sporulation. Shoots were scored as the most severe expression of symptoms found on any of the leaves. yTwo replications were performed for each entry, except where the entry is followed by an *, indicating a single replication. Identical results are indicated by a single number, discrepancies are indicated by listing both results. xNot tested. wNumber of cultivars inoculated with each isolate with no visible disease symptoms (rating of 1). vNumber of cultivars inoculated with each isolate showing a 2 or 3 reaction. uNumber of cultivars inoculated with each isolate showing a 4 reaction in at least one test.

554 HORTSCIENCE VOL. 39(3) JUNE 2004 to 14. In general, most isolates were not able to produce visible symptoms on about half of the tested cultivars. Notable exceptions to this were the three ‘Desirable’ isolates De-Tif-3, De-Mo-11, and Al-LI-DE that produced in- termediate reaction types on 14, 13, and 10 cultivars respectively. However, these isolates only produced susceptible reactions (class 4) on ‘Desirable’ or ‘Desirable’ and ‘Woodard’ in the case of AL-LI-DE. Interestingly, even though ‘Stuart’ is one of the founding cultivars of the southeastern pecan industry, and ac- counts for about ¼ the current pecan acreage (Florkowski et al., 2000), virulence to ‘Stuart’ was rare among the isolates tested (Table 2). This suggests there may be a form of stabiliz- ing selection acting to reduce the number of virulence genes in the pathogen. Five different ‘Desirable’ isolates were used to assess the effect of location on pathogen variation. As was noted above, isolate LA- MP-DE was likely to have been isolated from a cultivar other than ‘Desirable’ and so was not considered. The remaining four isolates shared some similarities. Three out of four were most virulent only on ‘Desirable’ and the remain- ing isolate AL-LI-DE was most virulent on ‘Desirable’ and ‘Woodard’. Each also had an Fig. 2. Microscopic examination of ‘Farley’ pecan leaves inoculated with four Cladosporium caryigenum intermediate reaction on ‘Cape Fear’, ‘Chey- isolates showing variation in the percent germinated conidia producing subcuticular hyphae. Each data enne’, ‘Farley’, ‘Pawnee’, and ‘Shoshoni’ and point represents the average of eight replicate leaves. Data points for each time period with a different was avirulent on ‘Barton’ and ‘Stuart’. This letter were significantly different, P < 0.05. suggests that in screening trials designed to provide maximum pathogen variation, prefer- as intermediate. Type 2 lesions produced pin- showed good resistance to most of the isolates. ence should be given to isolates from diverse point necrotic flecks and only rarely sporulated. Thus the isolates tested in this study are not genotypes over diverse locations. Type 3 lesions had restricted lesion growth, sufficient to accurately determine the field Comparison of these results with previ- reduced sporulation, and were surrounded susceptibility of all cultivars. ous studies is difficult due to differences in by a ring of chlorotic host tissue. A similar Isolates appear to have a narrow range the environment under which the disease range of symptoms has been reported in of cultivars on which they are most virulent. was assessed and in the rating systems used. the literature. Converse (1960) categorized Five isolates only produced a susceptible (type Bracewell (1996) and Turechek and Stevenson lesions into normal, yellow-margined, and 4) reaction on one cultivar, four produced a (1998) found that inoculum from a ‘Wichita’ fleck types. Bracewell (1996) reported that susceptible reaction on two cultivars, and the tree produced an intermediate reaction on when ‘Wichita’ and ‘Sumner’ isolates were remaining three isolates produced a suscep- ‘Sumner’. In this study, no visible symptoms cross-inoculated onto the other cultivar, lesions tible reaction on three, four, or five cultivars. were produced on ‘Sumner’ inoculated with were smaller, surrounded by a chlorotic halo, Generally, isolates were most virulent on Wi-Tif-2. This variance may be explained by and had restricted sporulation. Turechek and their cultivar of origin. The only exceptions pathogenic differences between the isolates Stevenson (1998) found that inoculum from to this were isolate St-Tif-13, obtained from a or by differences in the environment as the ‘Wichita’ trees produced smaller, yellow to ‘Stuart’ tree, which produced an intermediate previous experiments were conducted in a light brown lesions with significantly fewer reaction when inoculated back onto ‘Stuart’, greenhouse. Conner (2002) used the isolates spores per lesion and per lesion unit area on and isolate LA-MP-DE, obtained from a ‘Desir- De-Tif-3 and Wi-Tif-2 to inoculate the cultivars ‘Sumner’ leaves than they did when inoculated able’ tree, which did not produce any visible ‘Wichita’, ‘Desirable’, ‘Cape Fear’, and ‘El- onto ‘Wichita’ leaves. It thus appears to be reaction when inoculated onto ‘Desirable’. liot’ in the field. Each isolate only produced common for cross-inoculations to produce St-Tif-13 may represent an isolate obtained scab lesions on its cultivar of origin; however, atypical lesions with reduced size and conidia from a cultivar to which it is only partially only normal type 4 lesions were counted and production. Because resistance ranking order is adapted, as it was able to sporulate on ‘Stuart’. intermediate reactions were not reported. dependent upon the scab isolate tested (Table That LA-MP-DE did not produce any visible To determine the basis for the difference in 2) and a range of reaction types was observed, symptoms on ‘Desirable’ is more difficult lesion types, ‘Farley’ was inoculated with four resistance can be classified as vertical partial to explain. However, several other cultivars isolates, Fa-Tif-11, De-Tif-3, Pa-OK-11, and resistance (Vanderplank, 1984). were susceptible to this isolate suggesting Wi-Tif-2, and examined microscopically over All cultivars showed a differential sus- that the tree from which it was obtained may a 2-week period. These four isolates produced ceptibility to the isolates (Table 2). ‘Barton’, have been misidentified in the orchard. Often a range of disease reactions on ‘Farley’; no ‘Curtis’, and ‘Sumner’ were resistant to most when isolates produced a type 4 reaction on lesions for Wi-Tif-2, a 2 reaction for De-Tif- isolates, producing only a single type 2 reac- several cultivars those cultivars were related. 3, a 2 and a 3 reaction for Pa-OK-11, to a 4 tion to one of the isolates. These three cultivars For example, Ma-Tif-11 and LA-MP-DE reaction for Fa-Tif-11 (Table 2). are generally considered to have good field both produced type 4 reactions on ‘Kiowa’, Fa-Tif-11 produced significantly more resistance to scab (Sparks, 1992). Conversely, ‘Mahan’, ‘Schley’, and ‘Wichita’. All four subcuticular hyphae at each time period than ‘Wichita’ and ‘Schley’, cultivars rarely used cultivars are closely related as ‘Mahan’ is likely did the other three isolates (Fig. 2). Percent for new plantings because of their scab sus- a self of ‘Schley’, and is a parent of ‘Kiowa’, germinated conidia with subcuticular hyphae ceptibility (Sparks, 1992), were susceptible to and ‘Wichita’. increased with time to a maximum of 38% several of the isolates. However, ‘Cheyenne’, The number of cultivars tested in this on day 11. In contrast, De-Tif-3 increased to a cultivar that is very susceptible in the field, study resistant to each isolate varied from 3 a maximum of 15% at day 4 and Pa-OK-11

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Conner (2002) found race-specific re- produced no visible symptoms, produced sistance to be associated with a decreased halos at 20% of the infection sites by day 2 production of subcuticular hyphae and an and almost 80% of the infection sites by day increased production of a dark staining halo 4 (Fig. 5). Isolates De-Tif-3 and Pa-OK-11, in epidermal cells directly below the appres- which produced intermediate reactions, had sorium. Production of a halo around a cell wall halos associated with only 2% to 3% of the penetration or attempted penetration site is a infections sites at day 2 and 25% to 30% of common feature of induced resistance reactions the infection sites at day 4. Only by day 11 (Moerschbacher and Mendgen, 2000). ‘Farley’ for De-Tif-3 and day 15 for Pa-OK-11 were leaves inoculated with isolate Wi-Tif-2, which halos as common as they were in the Wi-Tif-

Fig. 4. Microscopic examination of ‘Farley’ pecan leaves inoculated with four Cladosporium caryigenum isolates showing variation in the percent germinated conidia producing subcuticular growth and repro- ductive initials. Each data point represents the average of eight replicate leaves. Data points for each time period with a different letter were significantly different, P < 0.05. Fig. 3. Development of Cladosporium caryigenum isolates on ‘Farley’ pecan leaves. (A) Isolate Fa- Tif-11, 11 d PI showing a extensive subcuticular growth and formation of reproductive initials. (B) Isolate Wi-Tif-2 4 d P.I. with darkened halo staining underneath the appressorium. (C) Isolate Pa-OK-11 15 d PI with restricted subcuticular growth surrounded by halo staining. Abbrevia- tions: a = appressorium, c = conidium, gt = germ tube, h = halo staining, ri = reproductive initials, sch = subcuticular hyphae. increased to a maximum of 10% at day 7, and both declined steadily to 2% to 4% by day 15. Only a small amount (≈1%) of subcuticular hyphae were detected at any time period in the Wi-Tif-2 inoculation. Subcuticular hyphae in each inoculation were monitored for the production of reproduc- tive initials which appear as pairs of melanized cells (Fig. 3A). Reproductive initials in the FA- Tif-11 inoculation were apparent after 11 d in 8% of the potential infection sites and nearly doubled to 15% of the sites by day 15 (Fig. 4). In contrast, reproductive initials were associated with <1% of sites in the De-Tif-3 inoculated leaves at day 15 and were not detected at any of the sites in the Pa-OK-11 and Wi-Tif-2 inoculated leaves. These results demonstrate Fig. 5. Microscopic examination of ‘Farley’ pecan leaves inoculated with four Cladosporium caryigenum the increased potential for spore production of isolates showing variation in the percent germinated conidia associated with a halo effect. Each data the susceptible reaction in comparison to the point represents the average of eight replicate leaves. Data points for each time period with a different intermediate and resistant reactions. letter were significantly different, P < 0.05.

556 HORTSCIENCE VOL. 39(3) JUNE 2004 2 inoculation. Fa-Tif-11, which produced a virulent on the cultivar over time. This leads found to be susceptible to scab in Mississippi. susceptible reaction on ‘Farley’, had the lowest to the well known boom and bust cycles en- Plant Dis. Rpt. 40:156. percent of infection sites associated with halo countered with the use of vertical resistance Crocker, T.F. 1996. Commercial pecan production in formation. By day 11 it had a similar percentage genes in plant breeding (Van der Plank, 1984). Georgia. Univ. Ga. Coop. Ext. Serv. Bul. 609 as Pa-OK-11 and by day 15 all isolates were The usefulness of a pecan cultivar with a new Demaree, J.B. and J.R. Cole. 1929. Behavior of Cladosporium effusum (Wint.) Demaree on some similar. However, by this time reproductive resistance gene will be largely determined by varieties of pecan. J. Agr. Res. 18:363–370. initials had begun to form (Fig. 4) and hyphal the durability of resistance and the cultivar’s Ellis, H.C., P. Bertrand, and T.F. Crocker. 2000. growth was extensive. inherent horticultural value. It seems reason- 2000 Georgia pecan pest management guide. Subcuticular hyphae were rarely observed able to assume that most resistance genes Univ. Ga. Coop. Ext. Serv. Bul. 841. in epidermal tissues showing dark halo staining will eventually be overcome by the pathogen Florkowski, W.J., G. Humphries, and T.F. Crocker. (Fig. 3C). This staining is likely associated if the cultivar is widely planted. When the 2000. Criteria used by Georgia growers in select- with modifications that slow or prevent fungal cultivar becomes susceptible, disease must be ing pecan cultivars—1998 pecan tree inventory. breakdown of plant cell walls (Moerschbacher controlled by fungicide and cultural methods. Proc. S.E. Pecan Growers Assn. 93:79–87. and Mendgen, 2000). The speed of the forma- At this point, the cultivar must have enough Gessler, C. and P. Blaise. 1994. Differential resistance in apple against scab and its use in breeding tion of this modification may be a major factor horticultural merits to compete with other and in orchard planting strategies to control in the eventual outcome of the reaction. This susceptible cultivars or it will be discarded the disease, p. 99–104. In. H. Schmidt and M. hypothesis is consistent with the observation by the grower. Kellerhals (eds.). Progress in temperate fruit that all four isolates had an equal percentage Durability of resistance may be improved breeding. Kluwer, Boston, Mass. of infection sites associated with halo staining by pyramiding functionally different resistance Goff, W.D., M. Nesbitt, R. Mullenax, F. Raspberry, by day 15, even though quite different fungal genes into a single cultivar. This may be an and B. Graves. 1998. Pest-resistant cultivars as a growth patterns were observed. A fast halo for- especially effective strategy in dealing with C. way to reduce input costs. Pecan S. 31(7):6–9. mation, as was seen in the Wi-Tif-2 inoculation, caryigenum given its apparent lack of a sexual Gottwald, T.R. 1982. of the pecan scab Cladosporium caryigenum was associated with an almost complete lack cycle. However, the formation of complex fungus . Mycologia 74:382–390. of subcuticular hyphae (Fig. 2) and no visible races capable of overcoming several resistance Guillebeau, P. 1998. What to do about the food qual- disease symptoms (Fig. 3B). Isolates De-Tif-3 genes may be hastened (Wolfe, 1993). Another ity protection act? Or how can we protect the and Pa-OK-11, associated with intermediate strategy would be to incorporate mixtures of pesticides we need?. Proc. S.E. Pecan Growers disease reactions, were slower than Wi-Tif-2 to cultivars containing different resistance genes Assn. 91:65–69. form halos (Fig. 5). In many cases, the growth into an orchard. Simulation models designed Moerschbacher, B. and K. Mendgen. 2000. Structural of subcuticular hyphae was restricted by dark for apple scab predict that a mixture of three aspects of defense, p. 231–277. In. A. Slusarenko, staining halos (Fig. 3C). In these cases, halo different cultivars with different resistance R.S.S. Fraser, and L.C. van Loon (eds.). Mecha- formation may have been sufficiently rapid genes could reduce the number of lesions after nisms of resistance to plant diseases. Kluwer, to reduce lesion size and sporulation, but not six generations by 65% when planted in alter- Boston, Mass. Sanderlin, R.S. 1992. Survey of Louisiana pecan enough to prevent evidence of symptoms. In nate rows, and by 79% in a within-row mixture orchards for scab pathogen populations tolerant the susceptible reaction with Fa-Tif-11, fungal (Gessler and Blaise, 1994). The development to benomyl fungicide. Proc. S.E. Pecan Growers growth was greatest. Many lesions had begun of new cultivars with similar horticultural Assn. 85:123–127. to form reproductive initials and extensive characteristics but different resistance genes Sanderlin, R.S. 1994. Effect of nut scab on pecan hyphal growth before any halo formation was would facilitate the adoption of this strategy yield and quality components, p. 45–58. In: M.W. seen. Halo formation in these cases was usually in pecan orchards. Smith, W. Reid, and B.W. Wood (eds.). Sustain- restricted to the outer edges of the lesion and ing pecan productivity into the 21st century. Proc. nd seldom encompassed the entire lesion resulting Literature Cited USDA–ARS 2 Natl. Pecan Wkshp. in less restricted hyphal growth. Sparks, D. 1992. Pecan cultivars: The Orchards Bracewell, C.J.R. 1996. Pathogenic variation of Foundation. Pecan Prod. Innovations, Watkins- The reservoir of resistance genes in C. il- Cladosporium caryigenum on resistant and ville, Ga. linoinensis seems to be large. Since pecan is susceptible pecan cultivars. MS thesis. Univ. Thompson, T.E. and L.J. Grauke. 1994. Genetic dichogamous, new combinations of resistance Ga., Athens. resistance to scab disease in pecan. HortScience genes are produced in each generation. This Conner, P.J. 1999. The Georgia pecan breeding 29:1078–1084. would explain why it is not uncommon for program. Proc. S.E. Pecan Growers Assn. Turechek, W.W. and K.L. Stevenson. 1998. Effects new seedlings to appear to be resistant for 92:77–80. of host resistance, temperature, leaf wetness, and several years or until planted on a wide scale, Conner, P.J. 2002. A detached leaf technique for leaf age on infection and lesion development of resulting in exposure to a virulent scab strain, studying race-specific resistance to Cladospo- pecan scab. Phytopathology 88:1294–1301. rium caryigenum in pecan. J. Amer. Soc. Hort. which then multiplies rapidly. Ephemeral Vanderplank, J.E. 1984. Disease resistance in plants. Sci. 127:781–785. Academic Press, Orlando, Fla. resistance is difficult to employ effectively in Converse, R.H. 1960. Physiologic specialization of Wolfe, M.S. 1993. Can the strategic use of disease re- monoculture orchard systems because of the effusum and its evaluation in vitro. sistant hosts protect inherent durability? p. 83–96. ability of the pathogen to adapt and become Phytopathology 50:527–531. In: Th. Jacobs and J.E. Parleviet (eds.). Durability Cole, J.R. and A.C. Gossard. 1956. Stuart pecan of disease resistance. Kluwer, Dordrecht.

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